interspecific aggressive behaviour by long-toed lapwings (vanellus crassirostris)

Anim. Behav., 1979, 27, 969-981

INTERSPECIFIC AGGRESSIVE BEHAVIOUR BY LONG-TOEDLAPWINGS (VANELL US CRASSIROSTRIS)

BY JEFFREY WALTERSAllee Laboratory of Animal Behavior, The University of Chicago, 5712 S. Ingleside Ave ., Chicago,

Illinois 60637

Abstract. In this paper interspecific aggression is related to ecological relationships between bird species .Three kinds of relationships are distinguished according to the presence or absence of aggression andthe degree to which resources are exclusively utilized : interspecific territoriality (aggression, exclusiveuse), partial exclusion (aggression, no exclusive use), and tolerance (no aggression, no exclusive use).Aggression by long-toed lapwings (Vanellus crassirostris) is examined within this framework, usingquantitative data gathered through observational sampling . Lapwings were interspecifically territorialwith one species, partially excluded five species, and tolerated four species . The results indicate that thefunction of interspecific aggressive behaviour may be related to competition, predation, or both .

Many birds direct aggressive behaviour towardnon-conspecifics intruding on their territories .Several explanations of this phenomenon havebeen proposed. First, interspecific aggressionmay be a means of competing with other species,especially for food (Orians & Willson 1964 ;Cody 1969 ; Cody & Brown 1970 ; Orians 1971 ;Lyon et al . 1977). Second, it may deter potentialpredators of eggs and small young, either directly(Jenni & Collier 1972 ; Graul 1975 ; Verner 1975 ;Slack 1976), or indirectly by reducing thedensity of prey for predators shared by theaggressive species and those species aggressedagainst (Myers in press). Finally, interspecificaggression usually occurs between species similarin plumage, voice, and display. The stimulipresented by some non-conspecifics may besufficiently similar to those presented by con-specifics to evoke an aggressive response from aterritory holder, although that response hasadaptive value only when directed towardconspecifics . Presumably, strong selectionagainst those that fail to respond to conspecificsleads to zealous responsiveness and hence tofrequent responses to inappropriate stimuli, i .e .errors of commission are a by-product of selec-tion against errors of omission (Simmons 1951 ;Hamilton 1962 ; Johnson 1963 ; Murray 1971 ;Emlen 1973 ; Post & Greenlaw 1975 ; Lill 1976) .The predation and competition hypotheses

are not mutually exclusive, and each hypothesismay be correct in some cases . Although thereare many examples of interspecific aggression inthe literature (e.g. Pitelka 1951 ; Udvardy 1951 ;Lanyon 1956 ; Orians & Collier 1963 ; Cody

969

1968 ; Orians &Horn 1969 ; Cheke 1971 ; Wolf &Wolf 1971 ; Gill & Wolf 1975 ; Schemske 1975 ;Morse 1976, in addition to above references), thegenerality of the hypotheses is not clear. At-tempts to explain interspecific aggression treatit as a single phenomenon, but it is apparentthat there are important differences amongcases of interspecific aggression. Specifically, theprobability that an intruder will be attacked andthe degree to which attacks exclude intrudersfrom the territory vary (e .g. contrast Gill & Wolf1975 and Lanyon 1956) . Below I shall categorizeinterspecific relationships and demonstrate theimportance of the resulting distinctions byexamining interspecific relationships involvinglong-toed lapwings (Vanellus crassirostris, Aves :Charadriidae) .

MethodsOrganisms and Study Site

The study was conducted in Amboseli Nation-al Park, Kenya, in July and August of 1975 . Thestudy site, particularly the vegetative composi-tion of lapwing habitat, is described in detailelsewhere (Walters in preparation). Briefly, thepark contains a mixture of short-grass plains andAcacia xanthophloea woodland surrounding twolarge marshes . Long-toed lapwings are restrictedto these marshes, and primarily inhabit surfacevegetation, such as Pistia and Ludwigia, overopen water .

Four pairs of lapwings and their young wereobserved nearly every day for 40 days, andseveral other pairs were observed intermittentlyduring the same period . Systematic sampling wasrestricted to a three-week period, and to one

970

family group consisting of two adults and fouryoung. Although long-toed lapwings lack conspi-cuous sexual dimorphism, the two adults in thisgroup were distinguishable from minor plumagedifferences . The sex of the adults was assumedfrom copulatory position . The subjects wereobserved by eye and with 7 x , 35-mm binocularsfrom a vehicle parked at the marsh's edge .

For comparative purposes, the study is dividedinto three periods termed, in chronologicalorder, the fledgling (first brood present), mating(first brood present, copulations leading tosecond brood), and nesting (first brood present,second clutch incubated) periods. The youngfirst attempted to fly at the end of the fledglingperiod, and were flying well by the last day of themating period .

Position SamplesLapwings were observed from 08 .00 to 18 .00

hours on 15 days . The position of each of the sixindividuals in the study group was recorded onthe hour and on the half-hour by scan sampling(Altmann 1974) (HPS, half-hourly positionscan, samples) . Positions were plotted on mapsof the study site that were produced by triangula-tion. In half of the hours of observation identicalscan samples also were conducted at 5, 10, 15, 20,35, 40, 45, and 50 min past the hour (PS, positionscan, samples).

Immediately following the PS samples at20 and 50 min past the hour, the positions of allbirds within the study site, other than the mem-bers of the study group, were recorded by scansampling (SS, species scan, samples) . The studysite was defined as the entire mapped area(approximately 1 . 4 ha), and included most of theterritory of the study group as well as some areasthat they did not utilize (see below) . Interactionsamples (next section below) were conductedduring these same hours, and jacana (Acto-philornis africanus) samples (second sectionbelow) were conducted in the remaining hours .Equal quantities of each type of sample wereaccumulated for each of the 10 hours of the dayfrom 08.00 to 18 .00 hours .

Interaction SamplesFrom 0 to 20 and from 30 to 50 min past the

hour, all aggressive behaviours by members ofthe study group were recorded ; each such 20-minperiod was one focal sample (Altmann 1974) onthe study group . The most frequent aggressivebehaviour was the `attack', in which the lapwingleft the substrate, flew rapidly toward an intruder,

ANIMAL BEHAVIOUR, 27, 4

swooped at it while uttering a harsh vocalization,and then returned to the substrate . Both a directflight path and a swoop were necessary for anevent to be recorded as an attack unless the`victim' fled before the lapwing reached it, inwhich case a rapid direct flight was sufficient. Inpractice attacks were easily distinguished fromother flights . If a lapwing swooped at morethan one victim in a single flight, one attackwas recorded for each victim . If two lapwingsattacked the same victim simultaneously, twoattacks were recorded. Events of the former kindwill be called `multiple attacks' ; the latter `jointattacks' .

The species of the victim, its initial position,and the result of the attack were recorded foreach attack. If a victim moved less than 5 mduring an attack, a result of 0 was recorded ; if itmoved 5 to 10 m, a 1 was recorded ; if it movedmore than 10 m, a 2 was recorded . Distanceswere estimated by eye and by reference to(scaled) maps. The interval in which the attackoccurred (i .e . the identity of the previous andsubsequent PS samples) and, in the case ofattacks on jacanas, the age-sex class of thevictim were also recorded . Age-sex classes usedwere adult male, adult female, and juvenile, thelatter being distinguishable from the others byplumage, and the first two being distinguishablefrom one another by size (McLachlan &Liversidge 1966) .

As a basis for subsequent statistical analysis,independence of attacks was examined asfollows. The average number of attacks per 5 minof interaction sampling was computed . If theattack rate is constant and attacks are indepen-dent, the expected number of 5-min periods inwhich there are 0, 1, 2, . . . oo attacks can beapproximated by the Poisson distribution,

xE(x) = N •

-e

X!

where x is the number of attacks in a 5-minperiod, N the total number of periods, a, theaverage number of attacks per period, and E (x)the expected number of periods in which thereare exactly x attacks . Each inter-PS sampleinterval represented one 5-min period of inter-action sampling ; 400 such intervals were accumu-lated . Because attack rate varied with the speciesattacked (see below), data for each species ofvictim were examined separately . Sample sizewas large enough to conduct a meaningfulcomparison of the observed and expected

distributions of attacks among 5-min periodsonly for attacks on jacanas : there was no signifi-cant deviation from the expected distribution(xs, P > 0 .05). The observed distributions ofattacks on squacco herons (Ardeola ralloides)and on blacksmith plovers (Vanellus armatus)were qualitatively similar to Poissons, but thaton waffled starlings (Creatophora cinerea) wasnot. In the latter case, attacks tended to occur inclusters, i.e there were more periods with two,three, or more attacks than expected . A violationof the independence assumption seems the mostlikely cause of this discrepancy . Overall, theresults of this analysis justify the use of theindependence assumption in subsequent analy-ses, but this discrepancy should be kept in mind .

Detailed descriptions were made of all aggres-sive interactions between lapwings and otherspecies that could not be classified as attacks . Thespecies involved, its initial position, the result ofthe interaction, and the behaviours employedwere recorded .

Interaction sampling had priority over posi-tion sampling: if an attack occurred during aPS sample, the sample was interrupted until allattack data were recorded . Similarly, PS sampleswere delayed if attacks were in progress when thesample was scheduled . (In practice such conflictswere infrequent because PS samples requiredonly 30 to 45 s to complete, and attack data wererecorded within 15 to 30 s of the termination ofan attack .) If the positions that birds occupiedfollowing attacks were not a random sample ofpositions occupied at other times, use of thisconvention biases the results of position samp-ling in favour of positions occupied followingattacks and against positions occupied duringattacks .

Jacana SamplesThe long-toed lapwing is ecologically very

similar to the African jacana. Data were collectedfrom jacanas residing in the study site so that thebehavioural relationship between these speciescould be studied in greater detail . In half of thehours of observation, two 10-min focal sampleson jacanas were taken . These samples wereseparated by an interval of at least 15 minand did not overlap with HPS samples . Ajacana located within the study site wasarbitrarily selected for each sample . The amountof time spent in each vegetation type (describedin Walters in preparation) and the locations ofattacks on the focal jacana were recorded . Theage-sex class of the focal jacana was noted, and

WALTERS : LAPWING AGGRESSION 971

the number of adult and young lapwings within20 m of it was recorded at the beginning, end,and half-way point of each sample.

ResultsGeneral Characteristics of Aggressive Behaviour

The attack was by far the most frequentlyobserved aggressive behaviour ; and like allother aggressive behaviours, it was performedonly by adult lapwings. Attacks were essentiallyspectacular threat displays : although the attackerswooped astonishingly close to its victim,victims were never actually touched. Mostaggressive interactions consisted of a singleattack, which either was ignored by the victim orcaused it to flee. Occasionally victims wereattacked a second time, and blacksmith ploversand jacanas sometimes retaliated when attacked .Retaliatory behaviours were usually defensive,typically consisting of a crouching posture withwings spread forward toward the attacker, butblacksmith plovers sometimes retaliated byattacking their attacker. Attacks by blacksmithplovers, which are congeners of long-toedlapwings, were extremely similar in form tothose of the lapwings.

The adult lapwings exhibited aggressivebehaviours other than attacks eight times . Threeof these involved violent physical contact,primarily striking the victim (a jacana in allthree cases) with the wings. The remaining fivecases differed from attacks in that repeatedswoops were made at the victim before thelapwing relanded, and that vocalizations inaddition to the usual one were emitted . Two ofthese interactions were with a harrier (Circusspecies), and three were with a coucal (Centropussuperciliosus) .

Harriers are predators of birds, especiallyyoung birds ; and coucals, which eat smallmammals and large insects (McLachlan &Liversidge 1966), are likely predators of eggs andsmall young, if not adults . Thus, responses tocoucals and harriers were probably anti-preda-tory in function . However, that responses tothese two species were similar, and different fromresponses to other species, does not necessarilyimply that responses to these two differed infunction from responses to other species,because aggressive behaviours are manifestationsof a causal, not a functional, system .

The analyses below are concerned only withattacks : other manifestations of aggression willnot be considered further. Thus, the remainder ofthe results section is a functional analysis of a

972

single behaviour . Whether an attack occurred aspart of a joint attack, part of a multiple attack,or as a `normal' attack did not affect the othercharacteristics of that attack : attacks in all thesecontexts are included in the analyses . Only onejoint attack, on a blacksmith plover, was ob-served. Nineteen multiple attacks were recorded,including two in which there were three victims .Fifteen of these, including both `triples', involvedonly jacana victims, and in another, one of thevictims was a jacana. One of the remainingmultiple attacks involved two squacco herons,one involved two wattled starlings, and oneinvolved two conspecifics . Often, but not always,victims in multiple attacks were near each other .The frequency of attacks by lapwings was

extremely high. In 2000 min of interactionsampling, 242 attacks on six species wereobserved, an average of one attack per 8 .3 min ofsampling. Three species of victims (jacanas,blacksmith plovers, and squacco herons) accoun-ted for 92% of all attacks, and jacanas aloneaccounted for 76 % . Black crakes (Limnocoraxflavirostra), wattled starlings, and long-tailedfiscal shrikes (Lanius cabanisi) were also attacked .

I

o LONG-TOED LAPWING • JACANA. BLACKSMITH PLOVER • GREBE. WHITE-BACKED DUCK • SHRIKEo SOUACCO HERON

POCHARDe o

0

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~ ~€a

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Fig . 1 . Spatial distribution of birds other than membersof the study group in the mating period, from SS samples .The figure includes the entire study site . The broken linedelimits the lapwings' territory .


Classes of RelationshipsThe spatial distribution of data points from

SS samples taken in the mating period is shownin Fig . 1 ; similar distributions were obtained inthe remaining periods . Throughout the study, allmembers of the study group confined theiractivities to the area enclosed by the dotted linein Fig . I plus an (unmapped) adjacent regionextending 30 m to the north ('zone A') . Otherlong-toed lapwings did not utilize these areasbut were found in adjacent areas (Fig . 1) . I shallrefer to this area, the enclosed region plus zoneA, as the study group's `territory', and shalljustify my use of that term in the discussion .

In Table I the number of times that otherspecies appeared in the lapwings' territory iscompared with the relative frequency with whichthese species were attacked. Based on these data,the relationships between these species andlapwings may be divided into three classes .Congenerics were attacked in and utilized areasadjacent to the territory, but not the territoryitself (class-l relationships). Jacanas, shrikes,crakes, starlings, and squacco herons wereattacked in and utilized both the lapwings'territory and adjacent areas (class-2 relation-ships). African pochards (Aythya erythrophthal-ma), common waxbills (Estrilda astrild), littlegrebes (Poliocephalus ruficollis), and white-backed ducks (Thalassornis leuconotus) utilizedboth the lapwings' territory and adjacent areas,but were not attacked (class-3 relationships)(Fig. 1 and Table I) . These relationships will nowbe examined in more detail.

Class-1 Relationships : Relationships with Black-smith Plovers

Most of the study group members' interac-tions with blacksmith plovers were with a pair ofplovers occupying an area adjacent to the lap-wings' territory . Initially, the plovers occupiedthe terrestrial portion of the study site, and thestudy group occupied the floating vegetationbeyond the submerged grass adjacent to theshore (Fig . 2). Both species utilized the submer-ged grass, but their ranges did not overlap, andthe lapwings attacked the plovers both in thesubmerged grass and in the floating vegetationjust adjacent to the submerged grass . Theplovers did not initiate any attacks, but theyfrequently 'counterchased' when attacked ; thatis, the plover initially fled aerially, but suddenlyboth the plover and the lapwing turned 1800 andthe plover chased the lapwing aerially in theopposite direction . The plover again turned, and

Table I. Relationships of Long-toed Lapwings with Other Species*

WALTERS: LAPWING AGGRESSION

*Based on 100 SS samples and 2000 min of interaction samples .

STUDY GROUP MEMBER =

NEIGHBORINGCONGENERIC =

ATTACK BY • ON • = o

A= FLOATING VEGETATIONB= SUBMERGED GRASSC= TERRESTRIAL GRASS

Fig . 2 . Territorial boundary between study group andcongeneric group to the northwest. Continuous linesdelimit the three vegetation types indicated in the key.Data points representing study group members are fromHPS samples, those representing attacks are from inter-action samples, and those representing blacksmithplovers are from SS samples . Symbols with an associatedarrow represent more than one data point, the number ofdata points represented being indicated by the associatednumeral .

both birds returned to their exclusively occupiedareas. By the end of the study, the lapwingsoccupied all of the submerged grass and someterrestrial habitat as well, and were attacking theplovers in parts of the remaining terrestrialhabitat (Fig. 2). Thus, attacks on plovers occur-red along the border between the area used bythe plovers and the area used by the study group .

These neighbouring congenerics did not fleewhen attacked ; in six of seven cases they movedless than 5 m .

Other pairs of long-toed lapwings had identicalrelationships with blacksmith plovers . Aggres-sion was always confined to borders betweenexclusively occupied areas, but was often moreintense and more frequent than that involvingthe study group. A variety of displays wereemployed by both species, in addition to attacks .

973

The similarity of the relationships of pairs oflong-toed lapwings with pairs of blacksmithplovers to the relationships of lapwings withconspecifics was striking. Each pair of lapwingsexclusively occupied, with respect to other pairs,a particular area (other lapwings were recorded155 times in SS samples, but only 4 times withinthe study group's territory ; see also Fig. 1), andaggression between pairs was largely confined tothe borders between such areas (see Figs. 3 and4 below) . Attacks were the most frequent form ofconspecific aggression (39 were recorded ininteraction samples), but other forms, includingvarious displays and beating each other withthe wings, were not uncommon .

Conspecifics occasionally flew into the studysite from elsewhere and attempted to land inareas occupied by resident pairs . These transientswere always attacked by the resident birds, andthey always then fled so far that they disappearedfrom my view. This response to aggressioncontrasted with the responses of resident lap-wings when attacked by neighbouring conspeci-fics : in 15 of 16 cases the victim moved less than5 m when attacked .

Class-2 RelationshipsGeneral description of species . Jacanas were

the most common species in the study site andwere, like lapwings, restricted to floating vegeta-tion. Although lapwings frequently attackedthem, jacanas were always present within thelapwings' territory (see Table I) . In fact, through-out the study two contiguous portions of thelapwings' territory were defended, each by asingle male jacana, against other male andjuvenile jacanas . One of these males built a nest

Relationshipclass Species

No. times recordedwithin lapwingterritory in SS

samples

Total No . timesrecorded in SS

samples

No. timesattacked ininteraction

samples

1 Blacksmith plover 1 32 182 Jacana 296 560 185

Squacco heron 44 72 19Wattled starling 7 8 10Black crake 2 3 3Shrike 7 11 3

3 White-backed duck 36 75 0Little grebe 32 36 0African pochard 2 2 0Waxbill 3 3 0

974


and incubated eggs within the lapwings' terri-tory. Other male jacanas were observed else-where within the territory, but it was not obviouswhether they were also defending territories . It islikely that female jacanas were defendingterritories that included the territories of one,two, or more males (this is the social system oftheir congener, Jacana spinosa ; see Jenni &Collier 1972) . The two male jacanas inhabitingthe lapwings' territory were frequently visited bya female jacana . Juvenile jacanas did not defendterritories but were frequent victims of aggres-sive behaviour by adult jacanas . Juvenilesseldom intruded into the lapwings' territory .The results of jacana samples showed that

jacanas were able to spend long periods of timewithin the lapwings' territory without beingattacked. Because focal jacanas were usuallywithin the lapwings' territory, the observedrates of attack on focal jacanas approximate therates of attack per unit time spent within theterritory . Roughly, a jacana was attacked oncefor every 12 min it spent within the territory ofthe lapwings . Jacanas were especially likely to beattacked in Wolff as and Azolla and were seldomattacked in Ludwigia ; the number of attacks ineach vegetation type was not proportional to theamount of time focal jacanas spent in thathabitat (x8 i P < 0 .05) .

Squacco herons also foraged extensively onfloating vegetation, but they were not alwayspresent at the study site, and they never occurredin numbers . They were recorded 50 times in SSsamples during the (study group's) fledglingperiod (mean = 1 . 09 birds per sample), 16 timesduring the mating period (mean = 0 .62), andonly six times during the nesting period (mean =0 .21). The number of times they were recorded

Species attacked

Squacco heronWattled starlingBlack crakeShrikeJacana (All age-sex classes)Jacana (Juvenile)Jacana (Adult Male)Jacana (Adult Female)

*Based on interaction samples .

Table II . Results of Lapwing Attacks (Class-2 Relationships)

during each period was not in proportion to thenumber of samples conducted in each period :they occurred more frequently than expectedduring the fledgling period and less frequentlythan expected during the nesting period (x2, P <0 .001) .

Long-tailed fiscal shrikes, wattled starlings,and black crakes foraged on floating vegetationonly occasionally. Small flocks of wattled star-lings often visited the study site during thefledgling period, but never thereafter . Thesebirds normally foraged in woodlands or plains,often in association with large mammals .Shrikes, too, were primarily terrestrial, but theyoccasionally forayed into the lapwings' territoryin pursuit of prey. Shrikes were present in theterrestrial habitat adjacent to the study sitethroughout the study. Crakes lived in the marsh,but they usually remained amid dense vegeta-tion, avoiding open habitat such as the floatingvegetation of the lapwings' territory . When theydid enter the territory, they fed there .Responses of intruders to attacks . Species

involved in class-2 relationships usually fledwhen attacked by lapwings (Table II), but theyfrequently returned to the territory soon afterfleeing from it . This contrasted with the beha-viour of blacksmith plovers, which did not fleewhen attacked (see above) . Squacco herons wereunusual in that they usually left the study sitewhen attacked and did not soon return, andjacanas were unusual in that they often did notflee when attacked . As is shown in Table II, thiswas characteristic of adult female jacanas, butnot of other age-sex classes of this species .Juvenile jacanas almost always left the lapwings'territory when attacked, and did not soonattempt to return. Males were variable in their

Results

No. of attacks

No. of attacks

No. of attacksduring which

during which

during whichvictim moved

victim moved

victim moved>lOm

5to10m

<5m

16 1 26 1 31 2 01 2 0

85 48 4833 21 219 8 9

1 4 19

responses to attacks, and often returned to theterritory soon after being evicted. Indeed,territorial male jacanas often returned to theterritory before the attacking lapwing hadalighted following the attack, running back intothe territory as quickly as they had run out .

Variations in frequencies of attacks . There wasconsiderable temporal variation in the frequencyof attacks on species with which lapwings hadclass-2 relationships . In order to determine thenature of this variation, the data were subjectedto a three-way analysis of variance . The depen-dent variable was the number of attacks per20-min interaction sample ; independent varia-bles were period, sex of the attacking lapwing,and density of intruders (the number of indivi-duals of species with which lapwings had class-2relationships recorded within the territory in theSS sample following the interaction sample inwhich the dependent variable was measured) .Although density is a continuous variable, it wascategorized as high (9 to 15 individuals), medium(7 to 8), or low (3 to 6) for purposes of analysis .The categories were chosen so that approxi-mately one of every three density measures fellin each category .

The results of the analysis are summarized inTable III. Clearly, the density of intruders had noeffect on the frequency of attacks . The twosignificant factors were period, attacks beingmost frequent in the fledgling period and be-coming progressively less frequent over themating and nesting periods, and the interactionbetween period and the sex of the attacker . Thenature of this interaction was that the effect ofperiod was much more pronounced on the

Table III . Three-way Analysis of Variance of Frequency of Lapwing Attacks on Class-2 Speciest


female lapwing than on the male . This sametrend was evident for attacks on blacksmithplovers, as is shown in Table IV . In addition, themale performed all territory defence (againstconspecifics) during the nesting period, whereasthis duty was shared in the previous periods . Insummary, the major source of temporal varia-tion in the frequency of attacks was a reductionin the frequency of attacks by the female lapwingas the young matured and the second clutch wasproduced .

The frequency of attacks did not vary diur-nally. The observed distribution of attacks amongthe 10 h of the sample-day did not differ signifi-cantly from the distribution expected under thehypothesis that attacks were equally likely at alltimes of the day (n = 240, yJ, p > 0 .20) .

There was a pronounced variation in thespatial distribution of attacks over time . Thespatial distributions of attacks during thefledgling and nesting periods are shown inFigs. 3 and 4, respectively . Nearly all attackswere confined to the lapwings' territory in allthree periods, but their distribution within theterritory was not constant. In the fledglingperiod, 58 % of the attacks on species involved inclass-2 relationships occurred in the area en-closed by solid lines in Fig . 3. The young con-fined all of their activities to this area during thefledgling period, and most (approximately 90 %)of their activities there during the other periods,whereas the adults avoided this area when feed-ing, but utilized it at other times (Walters inpreparation) . During the mating period, only18 % of the attacks on species involved in class-2relationships occurred in this area, and in the

975

t Variables are explained in the text. The symbols in parentheses in the first column show how the various sums of squareswere computed (SSA/B,C means SSA adjusted for the effects of B and C) . F ratio for factor i is equal to MSi /MSwithin cells. Three-way interaction was not tested . Significant factors are indicated by an asterisk .

Source of variationSum ofsquares(SS)

Degreesof

freedom

Meansquare(MS)

F ratio P value

Total (SStotai) 390. 11 99 3 .94 - -*Main effects + Interactions (SSbetween cells) 104 . 34 13 8 . 03 2 . 41 0 .008Residual (SSwithin cells) 285 .77 86 3 .32 - -*Total main effects (SSA,B,C) 45 .10 5 9 .02 2 . 71 0 . 025*Main effect : Period (SSA/B,c) 42 . 51 2 21 .26 6 . 40 0 . 003Main effect : Sex (SSB)A,C) 0 .81 1 0 . 81 0 . 24 0 . 623Main effect : Density (SSCJA,B) 1 . 36 2 0 .68 0 . 20 0 . 815

*Total interactions (SSbetween cells-SSA,B,C) 59 . 25 8 7 . 41 2 . 29 0 .033*Interaction : Period x Sex (SSABJBC,AC) 43 . 80 2 21 . 90 6 . 59 0 .002Interaction : Period x Density (SSACJAB,BC) 14 .84 4 3 .71 1 . 12 0 . 354Interaction : Sex x Density (SSsC/AB,AC) 2 . 37 2 1 . 18 0 . 36 0 . 701

976


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nesting period 18 % of such attacks occurredthere (Fig . 4) .

Attacks on these species during the nestingperiod occurred in the vicinity of the nest ratherthan in the area in which the young dwelled .During this period, 53% of the attacks werewithin 20 m of the nest (Fig . 4) . In contrast, only6 % of the attacks in the fledgling period occurredthere (Fig . 3) . The corresponding figure for themating period, 30 %, was intermediate betweenthose for the nesting and fledgling periods .

The differences among periods both in theproportions of attacks that occurred in thevicinity of the nest and in the area in which theyoung dwelled were statistically significant . Thedistribution among periods of attacks within 20m of the nest differed from the distributionexpected under the hypothesis that the propor-tion of attacks that occurred within 20 m of thenest was constant (x2, P < 0 .001), and thedistribution among periods of attacks within thearea in which the young dwelled differed fromthat expected under the hypothesis that a con-stant proportion of attacks occurred within thisarea (x2, P < 0 .001) .

J ACANA o LONG-TOED LAPWINGa COUCAL • BLACKSMITH PLOVER

o . WATTLED STARLINGo SOUACCO HERON

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977

The shift of attacks from the area in which theyoung dwelled to the vicinity of the nest was notcorrelated with any change in the distributionof the species attacked within the territory . Boththe correlation between the number of attackswithin the area in which the young stayed(measured in each interaction sample) and thedensity of species involved in class-2 relation-ships in this area (measured, as above, in thesubsequent SS sample), and the correlationbetween the number of attacks within 20 m ofthe nest and density of these species in thisregion, were near zero (r = 0 .09, r = 0 .07,respectively) and not significant (P > 0 .5) .

Although density of species involved in class-2relationships as a whole did not affect thefrequency of attacks by lapwings on these speciesas a whole, extreme variation in the density of aparticular species affected the attack rate on thatspecies . For example, correlated with the scarcityof squacco herons at the study site in the nestingperiod (see above) was a paucity of attacks onherons during that period . That all attacks onwattled starlings occurred during the fledglingperiod was a result of the complete absence ofstarlings from the study site during the otherperiods (see above) .

o LONG-TOED LAPWING*BLACKSMITH PLOVERoSQUACCO HERON∎ BLACK CRAKE JACANA -

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I o0

46

Fig . 4 . Spatial distribution of attacks in the nestingperiod. Remainder of key as in Fig . 3 .

978

The adult lapwing nearest an intruder wasmuch more likely to attack the intruder than wasthe other adult. From the position data in theimmediately preceding PS sample I determinedwhich of the adult lapwings was nearer eachattack victim just before the attack was launched.(Because of the low mobility of lapwings thismethod seldom results in error) . I examined onlythe first attack in each inter-PS sample interval .The nearer lapwing made the attack in 135 of163 attacks, a statistically significant result (two-tailed binomial test with p = 0 .5, P = < 0 .001) .The importance of proximity between an

attack victim and the attacking lapwing was alsoevident in jacana samples . Whether or not afocal jacana was attacked during a 5-min intervalwas independent of whether or not two or moreyoung lapwings were within 20 m of it at thestart of that interval (n = 180, xi, P > 0 .05), butwas not independent of whether or not an adultlapwing was within 20 m (y , P < 0.05). Attackswere more likely when an adult lapwing waswithin 20 m .

Class-3 RelationshipsThe lapwings were extremely tolerant of those

species that they did not attack, even near thenest and young. Little grebes and white-backedducks often remained in the lapwings' territoryfor several hours . Waxbills and pochards wereobserved at the study site only a few times, sotheir inclusion in this class must be regarded astentative .

Other SpeciesVarious other birds were neither recorded in

SS samples nor attacked in interaction samples(and thus their relationships with lapwings werenot classified), but were observed in the lapwings'territory at other times . These included fivespecies of aerial insectivores, four species ofsandpipers (Scolopacidae), and the sacred ibis(Threskiornis aethiopicus) . The sandpipers andibis were always attacked by the lapwings, butthe aerial insectivores never were .

DiscussionVariation in Aggressive Behaviour among Indivi-dual Lapwings

The quantitative data were based on only onelapwing family, but behaviour may vary betweenand within populations. It was necessary tosacrifice the ability to assess variation amongindividuals in order to obtain sufficient documen-tation of the relationships of a single lapwing


family. Although the rates of aggression anddifferences between the sexes in behaviourreported here cannot be assumed to be typical ofthe species, the qualitative relationships withother species can be . All observations of otherpairs of lapwings indicated that these other pairshad relationships identical to those of the studygroup with each of the other species described .

Proximate Causation of AttacksBlacksmith plovers were attacked whenever

they were perceived in or very near the territoryby the resident lapwings. Partially excludedspecies were nearly always present in the terri-tory, and thus available for attack . What, then,triggered attacks on these species? Visibility ofintruders was important, as attacks were usuallymade by the lapwing nearest the intruder ;attacks on jacanas were more likely in openareas (Wolffia, Azolla) than areas containingtaller, more dense vegetation (Ludwigia), andproximity of jacanas and adult lapwings madeattacks more likely . Furthermore, it seemed thatbirds flying to a new location, when returning tothe nest for instance, were especially likely tolaunch attacks . Similarly, Hall (1964) states thatattacks on other species by blacksmith plovers inSouth Africa are frequent just prior to andsubsequent to change-overs at the nest .

That a lapwing sighted an intruder did notguarantee an attack, however . Spatial cues andinternal state (i .e. reproductive stage) clearlyinfluenced the likelihood of attack (see above), yetother factors must also be involved, becauseeven during the fledgling period intruders some-times foraged near adult lapwings in areas whereattacks were most likely without being attacked .

Interspecific Relationships : Interspecific Terri-toriality, Partial Exclusion, and Tolerance

The term 'interspecific territoriality' has beenonly broadly defined previously . For example, itwas defined by Simmons (1951) as `persistentaggressive behaviour. . . showing some, if not all,of the reactions usually forthcoming in intra-specific encounters', and by Cody (1969) as`some area . . . defended at some time betweenspecies' . In effect, the term has been applied toall interspecific aggression involving territorialbirds . I propose to restrict the term to relation-ships such as those between long-toed lapwingsand blacksmith plovers because these relation-ships are similar to those intraspecific relation-ships to which the term (intraspecific) territori-ality is applied .

Both aggressive defence of space and exclusiveuse of space were characteristic of the relation-ships between long-toed lapwings and black-smith plovers . Aggressive defence is central toseveral recent definitions of (intraspecific) terri-toriality (e.g. Wilson 1971) ; exclusive use,regardless of the means by which it is achieved,is central to others (Pitelka 1959 ; Schoener 1968) .(Long-toed lapwings were intraspecifically terri-torial by either criterion) . I define interspecificterritoriality as a relationship between indivi-duals of different species characterized byexclusive use (with respect to each other) ofparticular areas, achieved by behavioural inter-actions including, but not restricted to, aggres-sive defence. Avoidance is another suitablemechanism by which exclusive use may beachieved. This definition excludes allopatry andhabitat selection, since these phenomena do notinvolve behavioural interactions betweenindividuals .

For cases of persistent aggressive behaviourbetween species, at least one of which is territor-ial, that do not result in exclusive use of an area(e .g. the lapwings' class-2 relationships), Ipropose the term `partial exclusion' . For cases ofsimultaneous use of space without aggression(e.g. the lapwings' class-3 relationships) Ipropose the term `tolerance' .

The Adaptive Significance of AttacksAlthough none of the three explanations of

interspecific aggression (see introduction) weretested directly, the results presented above enableone to evaluate the possible function(s) ofattacks .

All of the species attacked by lapwings may bea threat to eggs, but (with the exception ofsquacco herons and possibly blacksmith plovers)not to young. Conversely, all tolerated speciesare unlikely predators, even of eggs (see below) .Thus, it is possible that attacks served a directanti-predatory function, as did similar behaviourtoward coucals and harriers .

It is difficult to assess the possibility thatlapwing aggression reduces the density ofalternative prey (to lapwing chicks) of lapwingpredators, and thus indirectly reduces predationon chicks by rendering lapwing territories lessattractive as hunting grounds for lapwingpredators . First, aggression may not reduce thedensity of the species attacked, especially if oneconsiders lapwing habitat as a whole rather thanindividual territories (see below) . Second, thedata on lapwing predators are not sufficient to

WALTERS: LAPWING AGGRESSION 979

evaluate adequately the hypothesis that lapwingsselectively attack those species that share pre-dators with lapwing chicks. The species attackedby lapwings, with the notable exception ofsquacco herons, are comparable in size to lap-wing chicks, and are vulnerable to predationwhile on the substrate . One tolerated species, thewaxbill, is much smaller than young lapwings ;and the others, ducks and grebes, are relativelyinvulnerable to predators that take prey from thesubstrate because of their swimming and divingabilities .

All of the species attacked fed, at least occa-sionally, on insects on surface vegetation, as didlong-toed lapwings (see diets in McLachlan &Liversidge 1966) . Tolerated species either did notfeed on the surface vegetation (grebes), atevegetable matter (waxbills), or both (white-backed ducks) . This pattern is consistent with thehypothesis that attacks are a means of competingfor food .

The means by which aggressive behaviour mayaffect competition, should competition exist, isclear in the case of interspecific territoriality .Each pair of birds utilizes the resources, includ-ing food, within its area exclusively with respectto the other species . The effect of aggressiontoward partially excluded species on competitionbetween lapwings and these species for food isnot obvious. A mechanism by which aggressionaffects competition is needed for the competitionhypothesis to be viable in the case of partiallyexcluded species : one possible mechanism is thatattacks reduce the average density of attackedspecies below what it would be if aggressionwere absent. This hypothesis seems reasonablefor species, such as squacco herons, that areeasily evicted from the territory and do not soonreturn, but not for those, such as jacanas, thatare difficult to evict and, when evicted, soonreturn to the territory .

Congenerics are very similar to lapwings inappearance and voice, and it is possible thatlapwings mistook them for conspecifics . Thepartially excluded species, however, are verydifferent in plumage, display, and voice fromlapwings, and are not obviously more similar tothem than the tolerated species . It is difficult toreconcile this observation with the hypothesisthat interspecific aggressive behaviour is a by-product of resemblances between victims andconspecifics . Furthermore, these lapwings dem-onstrated an ability to make subtle discrimina-tions among species in their responses to aerialpredators (Walters in preparation) . Hence, it is

9 8 0


unlikely that they could not distinguish thespecies intruding on their territory from con-specifics, and considering the large amount oftime and energy expended attacking other speciesof birds, there would be strong selection to makesuch distinctions were it possible to do so .Spatial and temporal variation in attack

frequency provides some clues as to the functionof the behaviour. Attacks were clearly concen-trated in the vicinity of first the young and thenthe nest, which one would expect were attacks adirect deterrent to predators. That attacks wereconcentrated in the area in which the young fed isalso consistent with the competition hypothesis,but that they were later concentrated in thevicinity of the nest is not. Spatial variation inattack frequency could not be accounted for byvariation in space utilization by the adultlapwings, since adults avoided the area wheretheir young dwelled when attacks in that areawere most frequent .

The female ceased defending the territoryagainst conspecifics at the same time that sheceased attacking other species, as one wouldexpect were the mistaken identity hypothesisaccurate . However, this hypothesis cannotaccount for the spatial component of variation inattack frequency . Decreased aggression in themating and nesting periods is also compatiblewith a predation hypothesis, as the young areprobably less vulnerable to predation once theyfledge. It may also be compatible with thecompetition hypothesis, because the young ofmany bird species become more efficient feederswith age (Davies & Green 1976) and thus areless affected by competition with other species .

Finally, that attacks were most likely inWolfa and Azolla and least likely in Ludwigia iscontrary to what one might predict from thecompetition hypothesis, as the former vegetationtype is avoided by feeding birds, whereas thelatter is a preferred feeding area (Walters inpreparation).

The function of interspecific aggression bylapwings may be different from the function ofsimilar behaviour by other species, and may evendiffer in different relationships involving lap-wings. The function of interspecific aggressionmust be evaluated on a case-by-case basis .Interspecific territoriality should be distin-guished from partial exclusion in future studies .Previously, authors that have supported thecompetition hypothesis have discussed systemsthat appear to be interspecific territorialityrather than partial exclusion (Orians & Willson

1964 ; Cody 1969) . Conversely, those who havesupported the `mistake' hypothesis seem to beconsidering partial exclusion and not interspecificterritoriality (e .g. Johnson 1963 ; Post &Greenlaw 1975) . Making more subtle distinctionsamong relationships involving interspecific ag-gression may help clarify the function(s) of suchbehaviour .

AcknowledgmentsThis study was conducted during a field course inbehavioural biology offered at The University ofChicago. I wish to thank the other members ofthe course and the course instructors, Dr StuartAltmann and Dr Montgomery Slatkin, for theirassistance and encouragement . The course wasfunded by an NIMH training grant (MH 13936)and a grant from The Ridgeway Fund of TheUniversity of Chicago. Manuscript preparationwas funded by another NIMH training grant(MH 15181). I thank the Kenya Ministry ofTourism and Wildlife and Amboseli ParkWarden Mr. Joseph Kioko for their hospitalityand co-operation . Thanks are due to J. Altmann,Dr D. Cheney-Seyfarth, Dr A . W. Diamond,Dr G. Hausfater, Dr A . R. Kiester, Dr J . P.Myers, Dr F. A. Pitelka, Dr J. Rice, Dr R .Seyfarth, Dr M. Wade, and an anonymousreviewer for helpful comments on earlier draftsof the manuscript, and especially to Dr StuartAltmann, who painstakingly read each versionof the manuscript and offered most helpfulcriticism .

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WALTERS : LAPWING AGGRESSION 981

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(Received 1 February 1978; revised 31 August 1978 ;MS. number : A2136)

interspecific aggressive behaviour by long-toed lapwings (vanellus crassirostris)

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